Control of recurrent inhibition of the lateral posterior-pulvinar complex by afferents from the deep layers of the superior colliculus of the rabbit.

We investigated the effect of stimulation of the deep layers of the superior colliculus (SC) on the recurrent inhibition of the lateral posterior-pulvinar complex (LP) in anesthetized rabbits. Intracellular recordings from 23 relay cells in LP showed that they responded to SC stimulation with a long-lasting (140.2 +/- 19.6 ms; mean +/- SD) inhibitory postsynaptic potential (IPSP), which sometimes was followed by a rebound burst of spikes. The same SC stimulation evoked a burst of spikes in extracellular recordings from 31 recurrent inhibitory interneurons in the LP-cortical pathway, which were located in the ventral part of the visual sector of the thalamic reticular nucleus. The mean latency of the burst in reticular cells was 1.6 ms shorter than that of the IPSP in LP relay cells, suggesting that the IPSP in LP cells was mediated by these reticular cells. Intracellular recordings from nine reticular cells showed that the burst of spikes evoked by SC stimulation resulted from an excitatory postsynaptic potential that was always followed by a long-lasting (143.3 +/- 24.0 ms) IPSP. Stimulation of the contralateral predorsal bundle, the main output pathway of deep SC neurons, elicited similar responses in LP cells or reticular neurons with latencies longer than those from SC stimulation. The latency difference between the responses to predorsal bundle and SC stimulation is equal to the antidromic conduction time of predorsal bundle fibers, suggesting that the inhibition in LP originates from the activation of predorsal bundle-projecting neurons. The response characteristics of the inhibitory circuit of LP and of the lateral geniculate nucleus to SC stimulation are strikingly similar, implying that a similar circuit is used by predorsal bundle-projecting neurons to control the recurrent inhibition in both lateral geniculate nucleus and LP. Because the predorsal bundle-projecting neurons are believed to be involved in the initiation of saccadic eye movements, we suggest that the inhibitory circuits may play an important role in modulating ascending visual information during saccadic eye movements.

[1]  F. Reinoso-suárez,et al.  Connections to the lateral posterior-pulvinar thalamic complex from the reticular and ventral lateral geniculate thalamic nuclei: A topographical study in the cat , 1988, Neuroscience.

[2]  D. McCormick,et al.  Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro. , 1995, The Journal of physiology.

[3]  W. C. Hall,et al.  Collateral projections of predorsal bundle cells of the superior colliculus in the rat , 1989, The Journal of comparative neurology.

[4]  H. Swadlow,et al.  Thalamic inputs to visual areas 1 and 2 in the rabbit , 1986, The Journal of comparative neurology.

[5]  M. Deschenes,et al.  Striatal and cortical projections of single neurons from the central lateral thalamic nucleus in the rat , 1996, Neuroscience.

[6]  H Collewijn,et al.  Changes in visual evoked responses during the fast phase of optokinetic nystagmus in the rabbit. , 1969, Vision research.

[7]  J. Bourassa,et al.  Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer , 1995, Neuroscience.

[8]  Alexandre Pouget,et al.  Perceived geometrical relationships affected by eye-movement signals , 1997, Nature.

[9]  H. Collewijn,et al.  The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit , 1982, The Journal of comparative neurology.

[10]  C. Sawyer,et al.  The rabbit diencephalon in stereotaxic coordinates , 1954, The Journal of comparative neurology.

[11]  S E Petersen,et al.  Visual responses of pulvinar and collicular neurons during eye movements of awake, trained macaques. , 1991, Journal of neurophysiology.

[12]  H. Holländer,et al.  An autoradiographic study of the subcortical projections of the rabbit striate cortex in the adult and during postnatal development , 1979, The Journal of comparative neurology.

[13]  G. Krauthamer,et al.  Somatosensory neurons projecting from the superior colliculus to the intralaminar thalamus in the rat , 1990, Brain Research.

[14]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  Karl J. Friston,et al.  Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  J. Bourassa,et al.  Thalamic reticular input to the rat visual thalamus: a single fiber study using biocytin as an anterograde tracer , 1995, Brain Research.

[17]  D. Uhlrich,et al.  Histamine‐immunoreactive neurons and their innervation of visual regions in the cortex, tectum, and thalamus in the primate Macaca mulatta , 1996, The Journal of comparative neurology.

[18]  F. Duffy,et al.  Electrophysiological Evidence for Visual Suppression prior to the Onset of a Voluntary Saccadic Eye Movement , 1968, Nature.

[19]  S. Lindstro¨m.  Synaptic organization of inhibitory pathways to principal cells in the lateral geniculate nucleus of the cat , 1982, Brain Research.

[20]  W. Guido,et al.  Burst responses in thalamic relay cells of the awake behaving cat. , 1995, Journal of neurophysiology.

[21]  G. R. Wells,et al.  Visual projections to the pontine nuclei in the rabbit: Orthograde and retrograde tracing studies with WGA‐HRP , 1989, The Journal of comparative neurology.

[22]  C. W. Mohler,et al.  Saccadic suppression in the monkey , 1975, Vision Research.

[23]  Y. Kayama,et al.  Somatotopic organization in the rat thalamic reticular nucleus , 1984, Brain Research.

[24]  A K Moschovakis,et al.  Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. , 1988, Journal of neurophysiology.

[25]  S. Lindström.  Synaptic organization of inhibitory pathways to principal cells in the lateral geniculate nucleus of the cat. , 1982, Brain research.

[26]  S. Sherman,et al.  Relative contributions of burst and tonic responses to the receptive field properties of lateral geniculate neurons in the cat. , 1992, Journal of neurophysiology.

[27]  J. K. Harting,et al.  Projections of the superior colliculus to the supraspinal nucleus and the cervical spinal cord gray of the cat , 1982, Brain Research.

[28]  R. Guillery,et al.  Functional organization of thalamocortical relays. , 1996, Journal of neurophysiology.

[29]  H. Killackey,et al.  The Topographic Organization and Axis of Projection within the Visual Sector of the Rabbit's Thalamic Reticular Nucleus , 1989, The European journal of neuroscience.

[30]  K. Rockland.  Two types of corticopulvinar terminations: Round (type 2) and elongate (type 1) , 1996, The Journal of comparative neurology.

[31]  G. Ahlsén,et al.  Mutal inhibition between perigeniculate neurones , 1982, Brain Research.

[32]  B. Cleland,et al.  Organization of visual inputs to interneurons of lateral geniculate nucleus of the cat. , 1977, Journal of neurophysiology.

[33]  S. Sherman,et al.  Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: contributions of the low-threshold Ca2+ conductance. , 1992, Journal of neurophysiology.

[34]  A J Sefton,et al.  Connections between the reticular nucleus of the thalamus and pulvinar‐lateralis posterior complex: A WGA‐HRP study , 1995, The Journal of comparative neurology.

[35]  D. Paré,et al.  Thalamic collaterals of corticostriatal axons: Their termination field and synaptic targets in cats , 1996, The Journal of comparative neurology.

[36]  L. Towns,et al.  Projections of the dorsal lateral geniculate and lateral posterior nuclei to visual cortex in the rabbit , 1982, The Journal of comparative neurology.

[37]  S. Sherman,et al.  The projection of individual axons from the parabrachial region of the brain stem to the dorsal lateral geniculate nucleus in the cat , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  W Singer,et al.  Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. , 1977, Physiological reviews.

[39]  E. G. Jones,et al.  The morphology of physiologically identified GABAergic neurons in the somatic sensory part of the thalamic reticular nucleus in the cat , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  R. Giolli,et al.  An autoradiographic study of the projection of visual cortical area 1 to the thalamus, pretectum and superior colliculus of the rabbit , 1978, The Journal of comparative neurology.

[41]  David C. Burr,et al.  Compression of visual space before saccades , 1997, Nature.

[42]  D. Burr,et al.  Selective suppression of the magnocellular visual pathway during saccadic eye movements , 1994, Nature.

[43]  J. Zhu,et al.  Time Course of Inhibition Induced by a Putative Saccadic Suppression Circuit in the Dorsal Lateral Geniculate Nucleus of the Rabbit , 1996, Brain Research Bulletin.

[44]  G. Ahlsén,et al.  Inhibition from the brain stem of inhibitory interneurones of the cat's dorsal lateral geniculate nucleus. , 1984, The Journal of physiology.

[45]  Somatotopic organization in the rat thalamic reticular nucleus , 1985 .

[46]  S. Petersen,et al.  The pulvinar and visual salience , 1992, Trends in Neurosciences.

[47]  D. Munoz,et al.  Neuronal Activity in Monkey Superior Colliculus Related to the Initiation of Saccadic Eye Movements , 1997, The Journal of Neuroscience.

[48]  J. K. Harting,et al.  Connectional organization of the superior colliculus , 1984, Trends in Neurosciences.

[49]  J. Deniau,et al.  Spatio-temporal organization of a branched tecto-spinal/ tecto-diencephalic neuronal system , 1984, Neuroscience.

[50]  D. Fitzpatrick,et al.  Cholinergic and monoaminergic innervation of the cat's thalamus: Comparison of the lateral geniculate nucleus with other principal sensory nuclei , 1989, The Journal of comparative neurology.

[51]  L. Benevento,et al.  Single neurons with both form/color differential responses and saccade-related responses in the nonretinotopic pulvinar of the behaving macaque monkey , 1995, Visual Neuroscience.

[52]  Michael Conley,et al.  Organization of the Visual Sector of the Thalamic Reticular Nucleus in Galago , 1990, The European journal of neuroscience.

[53]  G. W. Beeler,et al.  Visual threshold changes resulting from spontaneous saccadic eye movements. , 1967, Vision research.

[54]  M. Bickford,et al.  Synaptic targets of cholinergic terminals in the pulvinar nucleus of the cat , 1997, The Journal of comparative neurology.

[55]  M. Pirchio,et al.  Cl‐ ‐ and K+‐dependent inhibitory postsynaptic potentials evoked by interneurones of the rat lateral geniculate nucleus. , 1988, The Journal of physiology.

[56]  M. Posner,et al.  Deficits in human visual spatial attention following thalamic lesions. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[57]  J. K. Harting.  Descending pathways from the superior colliculus: An autoradiographic analysis in the rhesus monkey (Macaca mulatta) , 1977, The Journal of comparative neurology.

[58]  D. V. van Essen,et al.  A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  P. Latour.  Visual threshold during eye movements , 1962 .

[60]  J R Huguenard,et al.  GABAB receptor‐mediated responses in GABAergic projection neurones of rat nucleus reticularis thalami in vitro. , 1996, The Journal of physiology.

[61]  D. LaBerge,et al.  Positron emission tomographic measurements of pulvinar activity during an attention task , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  D. Prince,et al.  Heterogeneous axonal arborizations of rat thalamic reticular neurons in the ventrobasal nucleus , 1996, The Journal of comparative neurology.

[63]  J. Zhu,et al.  Recurrent inhibitory interneurons of the Rabbit's lateral posterior-pulvinar complex. , 1997, Journal of neurophysiology.

[64]  M. Curtis,et al.  Electrophysiological characteristics of morphologically identified reticular thalamic neurons from rat slices , 1988, Neuroscience.

[65]  S. Petersen,et al.  Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation. , 1985, Journal of neurophysiology.

[66]  F. Lo,et al.  Physiological properties of the output neurons in the deep layers of the superior colliculus of the rabbit , 1995, Brain Research Bulletin.

[67]  E. G. Jones,et al.  Some aspects of the organization of the thalamic reticular complex , 2004, The Journal of comparative neurology.

[68]  D. Prince,et al.  Clonazepam suppresses GABAB-mediated inhibition in thalamic relay neurons through effects in nucleus reticularis. , 1994, Journal of neurophysiology.